Introduction

The Anthropocene marks the age of human impact on the globe as the steady decline of global biodiversity ushers in a mass extinction event [1,2]. Global biodiversity rates are steadily declining [3], and anthropogenic land modification and habitat loss seriously threaten the sustenance of terrestrial ecosystems [45–6]. Dirzo and Raven [7] assert that the loss of biodiversity is the one irreversible global environmental change our earth faces today. More studies are needed to improve global understanding of these developments.

Cycads are members of the Cycadales, the most threatened group of plant species on Earth [8910–11]. This Order of gymnosperms includes the families Cycadaceae, Stangeriaceae, and Zamiaceae, and includes more than 330 species [12]. Cycads are the most ancient of contemporary spermatophytes and encompassed approximately 20% of the world's flora during the Jurassic period [11, 13]. Research on today's cycad taxa can provide a direct window to the past and reveal the characteristics that have enabled the long persistence of this group [14].

In recent decades, numerous taxonomic revisions have focused on the entire Cycadales, its families, or its genera. Detailed evaluations of taxa in the Cycadales [1516–17] or the Cycadaceae [18] have examined variations in functional traits, providing a useful basis for comparing cycads as a group to global data sets. However, only a few papers examine the robust range of cycad species and traits in relation to global data sets.

A more comprehensive look at the world's most threatened plant group may improve our understanding of world-wide threats to global biodiversity. To our knowledge, the only detailed published assessments of the status of cycads were in 2003 [13, 19]. Since that time the International Union for Conservation of Nature's Red List of Threatened Species has been heavily refined and expanded (238 species in 2004 versus 303 species in 2014), with substantial and enduring cycad taxonomic revisions and assessments. Moreover, we are not aware of any recently published reports that include an intrinsic evaluation of the Red List database for all accepted contemporary cycad species. To address this research gap, we have conducted an empirical comparison of the IUCN Red List data (Red List hereinafter) of various cycad groupings. The commonalities and idiosyncrasies found could improve cycad conservation strategies on regional and global scales.

Methods

For taxonomic authority, we employed the most recently published World List [12]. We compared this list to the taxa included in the 2014 Red List to determine the proportion of accepted taxa successfully uploaded to the Red List. For each Red List entry, we created a database of the threat category and the core criteria used for determining the threat status. Threat categories included: critically endangered, endangered, vulnerable, near threatened, and least concern. The March to August 2014 database consisted of 337 entries, of which 303 were found on both the Red List and the World List. Entries on the Red List that were not confirmed on the World List were not included in our analyses. We used the database to evaluate overall trends among genera and threat categories by creating chi-square contingency tables with five approaches.

First, we organized the data into groups by threat category. We tallied the species within each genus that were listed under each threat category on the Red List. Then we added a group to include the species on the World List that were not found on the Red List, and these were added to the data as the category “not listed.” Second, we worked exclusively with the 303 valid species on the Red List and organized the data into groups by genera. We tallied the number of species within each threat category that were listed under each genus on the Red List. Third, we again organized the database into groups by threat categories. The species within each criterion [20] that were listed under each category were organized into a contingency table. Fourth, we organized the database into groups by genus, and the species within each criterion that were listed under each genus were organized into a contingency table. Lastly, we created a contingency table for each genus that incorporated the number of species on the Red List and the number of species not included on the Red List in order to identify which genera have been least evaluated.

Chi-square contingency table analysis was performed on the direct counts within each table using the PROC FREQ command in SAS V 9.2. This approach tested the hypothesis that the proportions of species observed in the groups within each genus or category were similar among genera or categories.

Discussion

Recent capabilities of assessing large data sets to illuminate general and global trends have enabled tools like ionomics [21], metabolomics [22], and web-based data analysis [23]. The Red List has been used for decades as a tool for cataloguing conservation status, for monitoring species, and for making decisions. With appropriate analysis, the robustness of the Red List is also useful for understanding global trends.

Arguing the merits and limitations of the Red List is beyond the scope of our paper, and has been done elsewhere [e.g., 24]. Formal methods for calculating Red List changes within any group of organisms have been established as the Red List Index (RLI) [25]. Because the RLI focuses exclusively on category changes within a group of organisms over time, limiting evaluations of Red List data to the RLI calculator may preclude interpretations based on independent unique assessments by conservationists. IUCN-endorsed formal assessments of species groups [e.g., 13, 26] are invaluable, but should not exclude the value of ad hoc evaluations of the quantitative data contained in the Red List. The importance of independent interpretations of Red List data can be seen in published assessments of various groups of organisms, such as birds [27], amphibians [28], marine turtles [29], and butterflies [30]. Our goal was highly exacting in addressing Red List data specific to the Cycadales in 2014. Several outcomes are noteworthy.

First, every means of interpreting the information in the Red List confirms that the world's living cycad species are exceedingly threatened. Of the 2014 Red Listed cycad species, almost two-thirds were threatened according to categories of the Red List. This confirms the 2010 assertions [11]. As more cycad species are newly described and taxonomic modifications clarify cycad classification, we believe the changes will universally increase the high threat categories and proportionally decrease the low threat categories. For example, the two most recently described Philippine Cycas species deserved Critically Endangered status as soon as they were described [31,32].

Second, the 34 missing species and the two Data Deficient species represent a deficiency in global cycad conservation efforts that should be corrected. The accurate assessment of international Cycadales conservation cannot be ascertained until all legitimately described taxa have been evaluated and added to the Red List by capable, informed local experts.

Third, the differences among the compared categories and genera were sizeable. No general trend emerged as canonical among our groupings within the Cycadales. For example, Encephalartos contained the greatest number of Critically Endangered species (Appendix 1), but was fourth on the list for Endangered species (Appendix 2). No other genus exhibited a similar pattern. Our findings underscore the fallacy of attempting to apply results from one genus or geographic region to other genera or geographic regions. For instance, Golding and Hurter [33] published a detailed assessment of the African Encephalartos species using Red List data, and suggested that continent-level actions are needed. Attempting to apply the African results to other continents would be useless based on our findings.

Fourth, the genera exhibiting Red List traits that may change the most in the near future can be envisaged from our results. Cycas, for example, contained roughly 40% of the species in the Near Threatened and Vulnerable categories. Because Cycas contains so many species in these “lower” threat categories, future changes in the Red List will cause a greater relative shift toward more threatened status for Cycas than for the other genera. Alternatively, about 65% of the Critically Endangered cycads were Encephalartos and Zamia species. These genera cannot exhibit a greater relative shift toward more threatened status on the Red List even if these Critically Endangered species become more threatened. Thus, studies that evaluate the global status of cycads need to be conducted routinely in accordance with changing IUCN assessments to best capture these impending changes.

Fifth, the alphanumerical assignments to category and criteria information contained within the Red List are not as useful for uncovering some of the causal reasons for assigning criteria. Most species descriptions include these underlying causes in the narrative portions of the listing. For example, assigning criteria based on decline in range may be caused by habitat loss from land conversion but also caused by invasive pests that generate local extirpations and population fragmentation. The IUCN has profiled two species that demonstrate these two contrasting threats to cycad conservation [11]. The conservation efforts needed to reverse these contrasting causes for the same criterion would not be similar.

Many cycad species have been exploited throughout the world for food, spiritual, and medicinal uses [11, 343536–37]. In some regions, the local cycad represents the potent cultural history of the indigenous people. Conserving these cycad species may also conserve traditional knowledge and cultural identity that are threatened by the loss of the cycad.

In summary, this straightforward technical assessment of the 2014 Red List cycad data may inform various aspects of global cycad conservation. Although every informed cycad biologist has a general understanding of the implications of our results, such widespread knowledge does little for posterity unless it is published in some form, especially if historical changes in taxonomic modifications and threat status become difficult to construct retrospectively. Conservationists may tend to focus their efforts exclusively on local species or nearby geographic regions, and thereby overlook global trends. This may lead to oversights in the significance of local knowledge and conservation efforts for global conservation strategies. Therefore, we believe a periodic overview of global data such as this paper is warranted. Our methods or any alternative empirical evaluations of the Cycadales database should be repeated periodically (in addition to the sanctioned RLI) to transfer the immense value of the evolving Red List into pragmatic outcomes of informed conservation practices. Osborne [38] suggested that a 10-year time scale is fitting for assessing cycad population changes. However, we believe this interval should be shortened to at most 5 years, given the increasing rate at which we are losing species and at which threats are arising and interacting.